Cnidocyte discharge is regulated by light and opsin-mediated phototransduction

David C Plachetzki,Caitlin R Fong,Todd H Oakley

doi:10.1186/1741-7007-10-17

David C Plachetzki, Caitlin R Fong + Show 1 more

Open Access

https://doi.org/10.1186/1741-7007-10-17

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Abstract

BackgroundCnidocytes, the eponymous cell type of the Cnidaria, facilitate both sensory and secretory functions and are among the most complex animal cell types known. In addition to their structural complexity, cnidocytes display complex sensory attributes, integrating both chemical and mechanical cues from the environment into their discharge behavior. Despite more than a century of work aimed at understanding the sensory biology of cnidocytes, the specific sensory receptor genes that regulate their function remain unknown.ResultsHere we report that light also regulates cnidocyte function. We show that non-cnidocyte neurons located in battery complexes of the freshwater polyp Hydra magnipapillata specifically express opsin, cyclic nucleotide gated (CNG) ion channel and arrestin, which are all known components of bilaterian phototransduction cascades. We infer from behavioral trials that different light intensities elicit significant effects on cnidocyte discharge propensity. Harpoon-like stenotele cnidocytes show a pronounced diminution of discharge behavior under bright light conditions as compared to dim light. Further, we show that suppression of firing by bright light is ablated by cis-diltiazem, a specific inhibitor of CNG ion channels.ConclusionsOur results implicate an ancient opsin-mediated phototransduction pathway and a previously unknown layer of sensory complexity in the control of cnidocyte discharge. These findings also suggest a molecular mechanism for the regulation of other cnidarian behaviors that involve both photosensitivity and cnidocyte function, including diurnal feeding repertoires and/or substrate-based locomotion. More broadly, our findings highlight one novel, non-visual function for opsin-mediated phototransduction in a cnidarian, the origins of which might have preceded the evolution of cnidarian eyes.

Highlights

Cnidocytes, the eponymous cell type of the Cnidaria, facilitate both sensory and secretory functions and are among the most complex animal cell types known
The cellular morphology of cnidocyte battery complexes In order to establish a morphological framework for comparing gene expression in the battery complexes of our study system H. magnipapillata, we explored the cellular composition of these structures using immunohistochemistry and confocal microscopy
These findings suggest that a ciliarytype phototransduction cascade comprised in part by opsin, cyclic nucleotide gated (CNG), and arrestin could play a role in the sensory regulation of cnidocyte discharge

Summary

Introduction

Cnidocytes, the eponymous cell type of the Cnidaria, facilitate both sensory and secretory functions and are among the most complex animal cell types known. In addition to their structural complexity, cnidocytes display complex sensory attributes, integrating both chemical and mechanical cues from the environment into their discharge behavior. Animal sensory systems provide a useful model for understanding the origins and evolution of complex traits. While a detailed understanding of the signaling pathways and cell types that function in the diversity of animal sensory systems is becoming increasingly common, most work in sensory molecular biology has been confined to an exceedingly small taxonomic sample of model bilaterian species. Arrestins, which act to quench phototransduction by binding activated opsin [13] are another common feature of bilaterian phototransduction pathways [14,15,16], but their involvement in cnidarian phototransduction systems has yet to be examined

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